scholarly journals Frontal eye field inactivation alters the readout of superior colliculus activity for saccade generation in a task-dependent manner

2019 ◽  
Author(s):  
Tyler R. Peel ◽  
Suryadeep Dash ◽  
Stephen G. Lomber ◽  
Brian D. Corneil
Keyword(s):  
Superior Colliculus ◽  
Oculomotor System ◽  
Frontal Eye Field ◽  
Frontal Eye Fields ◽  
Dependent Manner ◽  
Reversible Inactivation ◽  
Ensemble Coding ◽  
Intermediate Layers ◽  
Plausible Model ◽  
The Impact

AbstractSaccades require a spatiotemporal transformation of activity between the intermediate layers of the superior colliculus (iSC) and downstream brainstem burst generator. The dynamic linear ensemble-coding model (Goossens and Van Opstal, 2006) proposes that each iSC spike contributes a fixed mini-vector to saccade displacement. Although biologically-plausible, this model assumes cortical areas like the frontal eye fields (FEF) simply provide the saccadic goal to be executed by the iSC and brainstem burst generator. However, the FEF and iSC operate in unison during saccades, and a pathway from the FEF to the brainstem burst generator that bypasses the iSC exists. Here, we investigate the impact of large yet reversible inactivation of the FEF on iSC activity in the context of the model across four saccade tasks. We exploit the overlap of saccade vectors generated when the FEF is inactivated or not, comparing the number of iSC spikes for metrically-matched saccades. We found that the iSC emits fewer spikes for metrically-matched saccades during FEF inactivation. The decrease in spike count is task-dependent, with a greater decrease accompanying more cognitively-demanding saccades. Our results show that FEF integrity influences the readout of iSC activity in a task-dependent manner. We propose that the dynamic linear ensemble-coding model be modified so that FEF inactivation increases the gain of a readout parameter, effectively increasing the influence of a single iSC spike. We speculate that this modification could be instantiated by a direct pathway from the FEF to the omnipause region that modulates the excitability of the brainstem burst generator.Significance statementOne of the enduring puzzles in the oculomotor system is how it achieves the spatiotemporal transformation, converting spatial activity within the intermediate layers of the superior colliculus (iSC) into a rate code within the brainstem burst generator. The spatiotemporal transformation has traditionally been viewed as the purview of the oculomotor brainstem. Here, within the context of testing a biologically-plausible model of the spatiotemporal transformation, we show that reversible inactivation of the frontal eye fields (FEF) decreases the number of spikes issued by the iSC for metrically-matched saccades, with greater decreases accompanying more cognitively-demanding tasks. These results show that signals from the FEF influence the spatiotemporal transformation.

scholarly journals Modulation of Presaccadic Activity in the Frontal Eye Field by the Superior Colliculus

2009 ◽  
Vol 101 (6) ◽  
pp. 2934-2942 ◽  
Author(s):  
Rebecca A. Berman ◽  
Wilsaan M. Joiner ◽  
James Cavanaugh ◽  
Robert H. Wurtz
Keyword(s):  
Cerebral Cortex ◽  
Superior Colliculus ◽  
Eye Movement ◽  
Frontal Eye Field ◽  
Visual Response ◽  
Saccadic Eye Movement ◽  
Reversible Inactivation ◽  
Intermediate Layers ◽  
Eye Field ◽  
Neuronal Processing

A cascade of neuronal signals precedes each saccadic eye movement to targets in the visual scene. In the cerebral cortex, this neuronal processing culminates in the frontal eye field (FEF), where neurons have bursts of activity before the saccade. This presaccadic activity is typically considered to drive downstream activity in the intermediate layers of the superior colliculus (SC), which receives direct projections from FEF. Consequently, the FEF activity is thought to be determined solely by earlier cortical processing and unaffected by activity in the SC. Recent evidence of an ascending path from the SC to FEF raises the possibility, however, that presaccadic activity in the FEF may also depend on input from the SC. Here we tested this possibility by recording from single FEF neurons during the reversible inactivation of SC. Our results indicate that presaccadic activity in the FEF does not require SC input: we never observed a significant reduction in FEF presaccadic activity when the SC was inactivated. Unexpectedly, in a third of experiments, SC inactivation elicited a significant increase in FEF presaccadic activity. The passive visual response of FEF neurons, in contrast, was virtually unaffected by inactivation of the SC. These findings show that presaccadic activity in the FEF does not originate in the SC but nevertheless may be influenced by modulatory signals ascending from the SC.

scholarly journals FRONTAL EYE FIELD INACTIVATION DIMINISHES SUPERIOR COLLICULUS ACTIVITY, BUT DELAYED SACCADIC ACCUMULATION GOVERNS REACTION TIME INCREASES

2017 ◽  
Author(s):  
Tyler R. Peel ◽  
Suryadeep Dash ◽  
Stephen G. Lomber ◽  
Brian D. Corneil
Keyword(s):  
Reaction Time ◽  
Superior Colliculus ◽  
Neural Activity ◽  
Accumulation Rate ◽  
Frontal Eye Field ◽  
Frontal Eye Fields ◽  
Relevant Parameter ◽  
Intermediate Layers ◽  
Eye Field ◽  
Accumulator Models

AbstractStochastic accumulator models provide a comprehensive framework for how neural activity could produce behavior. Neural activity within the frontal eye fields (FEF) and intermediate layers of the superior colliculus (iSC) support such models for saccade initiation, by relating variations in saccade reaction time (SRT) to variations in parameters such as baseline, rate of accumulation of activity, or threshold. Here, by recording iSC activity during reversible cryogenic inactivation of the FEF in non-human primates, we causally test which parameter(s) best explains concomitant increases in SRT. While FEF inactivation decreased all aspects of ipsilesional iSC activity, decreases in accumulation rate and threshold poorly predicted accompanying increases in SRT. Instead, SRT increases best correlated with delays in the onset of saccade-related accumulation. We conclude that FEF signals govern the onset of saccade-related accumulation within the iSC, and that the onset of accumulation is a relevant parameter for stochastic accumulation models of saccade initiation.Significance StatementThe superior colliculus (SC) and frontal eye fields (FEF) are two of the best-studied areas in the primate brain. Surprisingly, little is known about what happens in the SC when the FEF is temporarily inactivated. Here, we show that temporary FEF inactivation decreases all aspects of functionally-related activity in the SC. This combination of techniques also allowed us to relate changes in SC activity to concomitant increases in saccadic reaction time (SRT). Although stochastic accumulator models relate SRT increases to reduced rates of accumulation or increases in threshold, such changes were not observed in the SC. Instead, FEF inactivation delayed the onset of saccade-related accumulation, emphasizing the importance of this parameter in biologically-plausible models of saccade initiation.

scholarly journals Impairment but not abolishment of express saccades after unilateral- or bilateral cryogenic FEF inactivation

2019 ◽  
Author(s):  
Suryadeep Dash ◽  
Tyler R. Peel ◽  
Stephen G. Lomber ◽  
Brian D. Corneil
Keyword(s):  
Superior Colliculus ◽  
Visual Information ◽  
Peak Velocity ◽  
Critical Role ◽  
Frontal Eye Fields ◽  
Visually Guided ◽  
Express Saccades ◽  
Cortical Input ◽  
Cortical Areas ◽  
Intermediate Layers

AbstractExpress saccades (ESs) are a manifestation of a visual grasp reflex triggered when visual information arrives in the intermediate layers of the superior colliculus (SCi), which in turn orchestrates the lower level brainstem saccade generator to evoke a saccade with a very short latency (∼100ms). A prominent theory regarding express saccades generation is that they are facilitated by preparatory signals, presumably from cortical areas, which prime the SCi prior to the arrival of visual information. Here, we test this theory by reversibly inactivating a key cortical input to the SCi, the frontal eye fields (FEF), while monkeys perform an oculomotor task that promotes ES generation. Across three tasks with a different combination of potential target locations and uni- or bilateral FEF inactivation, we found a spared ability for monkeys to generate ESs, despite decreases in ES frequency during FEF inactivation. This result is consistent with the FEF having a facilitatory but not critical role in ES generation, likely because other cortical areas compensate for the loss of preparatory input to the SCi. However, we did find decreases in the accuracy and peak velocity of ESs generated during FEF inactivation, which argues for an influence of the FEF on the saccadic burst generator even during ESs. Overall, our results shed further light on the role of the FEF in the shortest-latency visually-guided eye movements.New & NoteworthyExpress saccades (ESs) are the shortest-latency visually-guided saccade. The frontal eye fields (FEF) is thought to promote ES by establishing the necessary preconditions in the superior colliculus. Here, by reversibly inactivate the FEF either unilaterally or bilaterally, we support this view by showing that the FEF plays an assistive but not critical role in ES generation. We also found that FEF inactivation lowered ES peak velocity, emphasizing a contribution of the FEF to ES kinematics.

How the frontal eye field can impose a saccade goal on superior colliculus neurons

1992 ◽  
Vol 67 (4) ◽  
pp. 1003-1005 ◽  
Author(s):  
M. Schlag-Rey ◽  
J. Schlag ◽  
P. Dassonville
Keyword(s):  
Superior Colliculus ◽  
Frontal Eye Field ◽  
Intermediate Layers ◽  
Eye Field ◽  
Superior Colliculus Neurons

Saccades were electrically evoked from the frontal eye field (FEF) of two trained monkeys while saccade-cells were recorded from the intermediate layers of the superior colliculus (SC). We found that FEF microstimulation, eliciting saccades of a given vector, excited SC saccade-cells encoding the same vector and inhibited all others. Such a mechanism can prevent competing commands from arising simultaneously in different structures.

Enhancement of visual responses in monkey striate cortex and frontal eye fields

1976 ◽  
Vol 39 (4) ◽  
pp. 766-772 ◽  
Author(s):  
R. H. Wurtz ◽  
C. W. Mohler
Keyword(s):  
Receptive Field ◽  
Superior Colliculus ◽  
Visual Stimulus ◽  
Striate Cortex ◽  
Frontal Eye Field ◽  
Enhancement Effect ◽  
Frontal Eye Fields ◽  
Visual Response ◽  
Visual Responses ◽  
Response Enhancement

1. We have studied the visual enhancement effect in two areas of the cerebral cortex of monkeys. The response of the cells to a visual stimulus was determined both when the monkey used the visual stimulus as the target for a saccadic eye movement and when he did not. 2. In striate cortex cells with nonoriented, simple, complex, and hypercomplex receptive-field types were studied. Clear enhancement of the response to the appropriate visual stimulus was seldom seen when the monkey used the stimulus as a target for a saccade. In addition, any enhancement effect seen was nonselective; it occurred whether the monkey made a saccade to the receptive-field stimulus or some other stimulus at a point distant from the receptive field. The enhancement also occurred whether the monkey made a saccade to the stimulus or just released the bar when the stimulus dimmed. 3. This nonselective enhancement in striate cortex is in striking contrast to the selective enhancement of the visual response seen in the superior colliculus. The different characteristics of the enhancement in striate cortex and the observation of enhancement in the colliculus following ablation of striate cortex suggest that this cortical area is an unlikely source of the collicular enhancement. 4. These observations reinforce the distinction between striate cortex and superior colliculus. Striate cortex is an excellent analyzer of stimulus characteristics but a poor evaluator of stimulus significance. The superior colliculus is an excellent evaluator but a poor analyzer. 5. The area of frontal eye fields in which cells have clear visual responses has been better localized. Enhancement of the visual response of these cells also occurs and, at least for some cells, the response enhancement is selective. The response enhancement, like the visual properties of these frontal eye field cells, appears to be more closely related to the properties of superior colliculus cells than to striate cortex cells.

scholarly journals Bilateral saccadic deficits following large and reversible inactivation of unilateral frontal eye field

2014 ◽  
Vol 111 (2) ◽  
pp. 415-433 ◽  
Author(s):  
Tyler R. Peel ◽  
Kevin Johnston ◽  
Stephen G. Lomber ◽  
Brian D. Corneil
Keyword(s):  
Visual Cues ◽  
Brain Area ◽  
Reaction Times ◽  
The Other ◽  
Frontal Eye Field ◽  
Visually Guided ◽  
Reversible Inactivation ◽  
Eye Field ◽  
And Performance ◽  
The Impact

Inactivation permits direct assessment of the functional contribution of a given brain area to behavior. Previous inactivation studies of the frontal eye field (FEF) have either used large permanent ablations or reversible pharmacological techniques that only inactivate a small volume of tissue. Here we evaluated the impact of large, yet reversible, FEF inactivation on visually guided, delayed, and memory-guided saccades, using cryoloops implanted in the arcuate sulcus. While FEF inactivation produced the expected triad of contralateral saccadic deficits (increased reaction time, decreased accuracy and peak velocity) and performance errors (neglect or misdirected saccades), we also found consistent increases in reaction times of ipsiversive saccades in all three tasks. In addition, FEF inactivation did not increase the proportion of premature saccades to ipsilateral targets, as was predicted on the basis of pharmacological studies. Consistent with previous studies, greater deficits accompanied saccades toward extinguished visual cues. Our results attest to the functional contribution of the FEF to saccades in both directions. We speculate that the comparative effects of different inactivation techniques relate to the volume of inactivated tissue within the FEF. Larger inactivation volumes may reveal the functional contribution of more sparsely distributed neurons within the FEF, such as those related to ipsiversive saccades. Furthermore, while focal FEF inactivation may disinhibit the mirroring site in the other FEF, larger inactivation volumes may induce broad disinhibition in the other FEF that paradoxically prolongs oculomotor processing via increased competitive interactions.

Reversible Inactivation of Monkey Superior Colliculus. II. Maps of Saccadic Deficits

1998 ◽  
Vol 79 (4) ◽  
pp. 2097-2110 ◽  
Author(s):  
Christian Quaia ◽  
Hiroshi Aizawa ◽  
Lance M. Optican ◽  
Robert H. Wurtz
Keyword(s):  
Visual Field ◽  
Superior Colliculus ◽  
Large Fraction ◽  
Companion Paper ◽  
Initial Direction ◽  
Null Direction ◽  
Reversible Inactivation ◽  
Intermediate Layers ◽  
Visual Hemifield ◽  
Qualitative Estimate

Quaia, Christian, Hiroshi Aizawa, Lance M. Optican, and Robert H. Wurtz. Reversible inactivation of monkey superior colliculus. II. Maps of saccadic deficits. J. Neurophysiol. 79: 2097–2110, 1998. Neurons in the superior colliculus (SC) are organized as maps of visual and motor space. The companion paper showed that muscimol injections into intermediate layers of the SC alter the trajectory of the movement and confirmed previously reported effects on latency, amplitude, and speed of saccades. In this paper we analyze the pattern of these deficits across the visual field by systematically comparing the magnitude of each deficit throughout a grid of targets covering a large fraction of the visual field. We also translate these deficits onto the SC map of the visual/movement fields to obtain a qualitative estimate of the extent of the deficit in the SC. We found a consistent pattern of substantially increased saccadic latency to targets in the contralateral visual hemifield, accompanied by slight and inconsistent increases and decreases for saccades to the ipsilateral hemifield. The initial and peak speed of saccades was reduced after the injection. The postinjection amplitude of the saccades were either hypometric or normometric, but rarely hypermetric. Although errors in the initial direction of the postinjection saccades were small, they consistently formed a simple pattern: an initial direction with minimal errors (a null direction) separating regions with clockwise and counterclockwise rotations of the initial direction. However, the null direction did not go through the center of the inactivated zone, as would be expected if the SC alone were determining saccade direction, e.g., with a population code. One hypothesis that can explain the misalignment of the null direction with the lesion site is that another system, acting in parallel with the SC, contributes to the determination of saccadic trajectory.

scholarly journals Reversible Inactivation of Monkey Superior Colliculus. I. Curvature of Saccadic Trajectory

1998 ◽  
Vol 79 (4) ◽  
pp. 2082-2096 ◽  
Author(s):  
Hiroshi Aizawa ◽  
Robert H. Wurtz
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
Superior Colliculus ◽  
Saccadic Eye Movements ◽  
Cell Types ◽  
Neuron Activity ◽  
Eye Position ◽  
Two Dimensional ◽  
Reversible Inactivation ◽  
Intermediate Layers

Aizawa, Hiroshi and Robert H. Wurtz. Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. J. Neurophysiol. 79: 2082–2096, 1998. The neurons in the intermediate layers of the monkey superior colliculus (SC) that discharge before saccadic eye movements can be divided into at least two types, burst and buildup neurons, and the differences in their characteristics are compatible with different functional contributions of the two cell types. It has been suggested that a spread of activity across the population of the buildup neurons during saccade generation may contribute to the control of saccadic eye movements. The influence of any such spread should be on both the horizontal and vertical components of the saccade because the map of the movement fields on the SC is a two-dimensional one; it should affect the trajectory of saccade. The present experiments used muscimol injections to inactivate areas within the SC to determine the functional contribution of such a spread of activity on the trajectory of the saccades. The analysis concentrated on saccades made to areas of the visual field that should be affected primarily by alteration of buildup neuron activity. Muscimol injections produced saccades with altered trajectories; they became consistently curved after the injection, and successive saccades to the same targets had similar curvatures. The curved saccades showed changes in their direction and speed at the very beginning of the saccade, and for those saccades that reached the target, the direction of the saccade was altered near the end to compensate for the initially incorrect direction. Postinjection saccades had lower peak speeds, longer durations, and longer latencies for initiation. The changes in saccadic trajectories resulting from muscimol injections, along with the previous observations on changes in speed of saccades with such injections, indicate that the SC is involved in influencing the eye position during the saccade as well as at the end of the saccade. The changes in trajectory when injections were made more rostral in the SC than the most active burst neurons also are consistent with a contribution of the buildup neurons to the control of the eye trajectory. The results do not, however, support the hypothesis that the buildup neurons in the SC act as a spatial integrator.

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